Enhancing Biological Control With Insectary Plantings

Final Report for SW99-061

Project Type: Research and Education
Funds awarded in 1999: $83,929.00
Projected End Date: 12/31/2003
Matching Non-Federal Funds: $13,651.00
Region: Western
State: Oregon
Principal Investigator:
John Luna
Oregon State University
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Project Information

Summary:

Summary
We have conducted on-farm experiments in Oregon broccoli production systems to explore the potential of using insectary flowers to enhance the biological control of cabbage aphid (Brevicoryne brassicae) by naturally-occurring predacious hoverflies. Our conclusions include:
Insectary plantings increase abundance of hoverfly predator eggs in broccoli fields, however no suppression of cabbage aphid was demonstrated.
Both pest and beneficial insect species utilize nectar and pollen from the insectary plants we tested. The use of certain insectary plants may actually increase pest problems. Using beneficial insectary plantings for conservation biological control must consider impacts on pests, beneficials, and hyperparasitoids across all crops occurring within the system.
Selected insectary plants exhibit preferential attractiveness among entomophagous and pest species.
Biological pest control efforts need to be conducted at the species level of ecological inquiry, with considerable error possible from decisions made at the family level of taxonomic groupings.
Appropriate scale of experimental design needs to incorporate dispersal behaviors of target species and natural enemies.
Oviposition (egg-laying) behavior of adult entomophagous species may be key factor limiting effective biological control

Project Objectives:

1. To evaluate the relative attractiveness of selected insectary plants to entomophagous arthropods and key insect pests
2. To evaluate the potential of using beneficial insectary plants to enhance biological control of specific insect pests in broccoli production systems, including: the cabbage aphid complex and the worm complex.
3. To develop a multi-faceted educational program for growers and agricultural professionals on integrating beneficial insectary plantings into various kinds of farming operations to enhance biological pest control.

Introduction:

A recent report by the Consumers Union (1998) on the risk to children by pesticide residues in fruit and vegetables underscores continued widespread concerns for pesticide impacts on food safety and on non-target organisms in the environment. Although the concept of “integrated control,” introduced by Stern et al. (1959), called for an integration of a variety of biological, cultural, as well as chemical pest control measures, little progress has been made in the nearly 40 years since then to effectively integrate biological control into vegetable production systems (Luna and House, 1990). The largest obstacle to realizing this goal has not been lack of biological control options; rather the strict ‘quality’ standards demanded by buyers has necessitated rather intensive pesticide application programs for vegetable crops. Insect contamination standards in the food processing industry are even higher than in the fresh market, since processed food products are shipped globally in large containers and a rejected container load reverberates throughout the marketing chain. Processors react by demanding “bug-free” product from their growers.
Broccoli is a major vegetable crop grown by Oregon and California farmers. Broccoli is a particularly “pest rich” crop, attacked by cabbage root maggots, flea beetles, cucumber beetles, two species of aphids and at least four species of caterpillars. Conventional broccoli growers in Oregon rely primarily on synthetic pyrethroid insecticides for insect control.
Beneficial insectary plantings, a form of natural enemy augmentation, offer a promising opportunity to enhance the effectiveness of biological control in integrated production systems. Beneficial insectary planting refers to the intentional, planned introduction of selected flowering plants in agricultural ecosystems to increase nectar and pollen resources for natural enemies of insect pests. Many species of insect predators and parasitoid rely on pollen and nectar for their survival and reproductive success (Schneider, 1948; van Emden, 1962). Weed management practices, tillage, and other farming practices often produce agricultural systems that are florally impoverished, particularly during critical times in the life cycles of natural enemies when pollen and nectar resources are needed.
Two major groups of entomophagous insects (those predatory and parasitic insects that feed on other insects) that have been shown to be favorably affected by beneficial insectary plantings are the hover flies (Diptera: Syrphidae) (Wratten and van Emden, 1995) and the parasitic Hymenoptera (Powell, 1986). Pollen serves as source of protein and provides amino acids required for sexual maturation (Schneider, 1948) and nectar serves primarily as an energy resources providing carbohydrates. Adult hoverflies and parasitic wasps exhibit a high degree of selectivity for the flowers from which they feed (Leius, 1960; Cowgill et al., 1993). Attractiveness also differs between males and females, probably due to varied resource needs (Hickman and Wratten, 1996). The relative qualities of different pollens have also been shown to influence fecundity rates in hoverflies (Ankersmit et al., 1986).
The potential to enhance biological pest management through the use of beneficial insectary plantings has been clearly demonstrated in various agronomic and horticultural cropping systems (see next section for brief discussion of this work). However, an understanding of the seasonal phenology of the target pest is crucial and whether this critical period of control synchronizes with the blooming time of the insectary flower and the phenology of natural enemy species. Successful integration of a beneficial insectary planting into a particular farming system also requires an understanding of how it will fit into the overall management scheme of that system. Different kinds of insectary plants may be better suited to different farming systems.
To actually enhance biological pest control in a specific pest/crop situation, specific beneficial insectary plants must provide floral resources to specific natural enemies which are preying on the targeted pest or pests of concern (Gurr et al. 1998). In the work reported here, we focus on manipulating beneficial insectary plantings to enhance biological control of specific target insect pests in an annual row crop system (broccoli). In the broccoli system, we have focused on biological control of the cabbage aphid (Brevicoryne brassicae) and the green peach aphid (Myzus persicae),. These insect pests are widely distributed in many parts of North America and the world and strategies for enhancing biological control of these pests could have widespread impact. We have also expanded on earlier work (Colley and Luna, 2000) evaluating the relative preference of selected insectary plants by hoverflies and other insect pests.

Cooperators

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  • Mario Ambrosino
  • Bill Chambers
  • Paul Jepson

Research

Materials and methods:

Objective 1. To evaluate the relative attractiveness of selected insectary plants to entomophagous arthropods and key insect pests
Experimental Approach, Design and Methods
Field Sites: Two field experiment sites were established at two locations of Stahlbush Island Farm in late May 2000. Site 1, the “North site” was located at the main branch of Stahlbush Island Farm near Corvallis, OR. The flowers were planted 25 days after transplanting broccoli. Site 2, the “South site” was located at the South branch of Stahlbush Island Farm near Eugene, OR. The flowers were planted there 8 days after transplanting broccoli.
At each site, experimental treatments consisted of four species of insectary plants, including alyssum (Lobularia maritima), coriander (Coriandrum sativa), buckwheat (Fagopyrum esculentum) and phacelia (Phacelia tanacetifolia). Insectary crops were planted in 2 m x 5.5 m plots, with plots randomly arranged within the three replication blocks. The total strip length of the experiment was 66m in each trial. Alyssum and coriander were transplanted in five rows in each plot, with a within-row spacing of 40 cm between plants. Buckwheat and phacelia were sown in nine rows in each plot, and thinned to 15 cm within-row spacing. Planting dates were May 23, 2000 at the North trial, and on May 24 at the South trial. Insectary blocks were located adjacent to commercial fields of broccoli (see Objective 2 below for more details on the broccoli planting).
We used direct observation to quantify flower visiting by hoverfly species and other key natural enemies and insect pests. These other arthropods included lygus bug (Lygus hesperus), western spotted cucumber beetle (Diabrotica undecimpunctata undecimpunctata), imported cabbage worm (Pieris rapae), lady beetles, damsel bugs and green lacewings.
Objective 2. To evaluate the potential of using beneficial insectary plants to enhance biological control of specific insect pests in broccoli production systems, including: the cabbage aphid complex and the worm complex.
2000 Research. The same two experimental sites with the flower strips described above were used for this objective. To test whether the insectary block was affecting pests and natural enemies in the broccoli crops, two treatments were examined: “near to flowers” (within 15m), and “far from flowers” (more than 150m away from flowers). Broccoli plants sampled in each of these treatments were not treated with insecticides in a total area of 66m x 15m.
Fifty plants in each treatment block were randomly sampled every 4 days, starting with the sowing date of flowers, and ending at the last broccoli harvest. Whole plants were inspected and numbers per plant of each of the following key arthropod species and groups were recorded over this period: cabbage aphid (CA), green peach aphid (GPA), potato aphid, imported cabbage worm (ICW), cabbage looper, diamond back moth, hoverfly larvae and eggs, Cecidomyiid flies, aphid mummies, spiders, lady beetles, and lacewings.
In order to more accurately characterize the oviposition response of hoverflies to the various aphid colony sizes, types and locations, data collection was further refined to numbers per leaf. This detailed sampling method was started before hoverfly eggs began to appear, and as the architecture of the broccoli plants increased in complexity.
At harvest, 100 heads were randomly selected from each of the treatments in each of the trials and examined for the organisms mentioned above by detailed destructive sampling. This involved carefully breaking the heads into 1cm2 sections and looking for arthropods in these pieces for a period of 5 minutes per head.
2001 Research: The following Sub-objectives were established for Objective 2:
1. To quantify the within-field effect that added flowering plants have on the attraction and oviposition activities of hoverflies, and on the abundance of other arthropod natural enemies and herbivores in broccoli.
2. To evaluate the prey-finding and oviposition behaviors of adult hoverflies in commercial broccoli fields.
3. To evaluate the ability of hoverflies to limit populations of aphids in controlled conditions.
Sub-objective 1. To quantify the within-field effect that added flowering plants have on the attraction and oviposition activities of hoverflies, and on the abundance of other arthropod natural enemies and herbivores in broccoli.
An experiment was established in a 160 x 400 m broccoli field at Stahlbush Island Farm, 3 km East of Corvallis, OR. Winter season vegetation was killed with Roundup in March 2001, and a strip-tillage machine used to till 4 cm wide strips on 0.9 m centers. Broccoli was transplanted on May 28 along with a soil incorporation of Neemix and Goal (Oxyflourfen). An 18 m (= 20 row) block of broccoli (running the whole 400 m length of the field) was left untreated with the aphicides which were applied to the rest of the field (Provado 43 days after transplant and Pyrin 67 days after transplant). This block was 90 m from one border and 50 m from the border of the other side. Two insecticide applications were made for lepidopteran pests, to the strip and the rest of the field (Confirm 43 days after transplant and Success 67 days after transplant).
Within the 18 x 400 m strip, two “insectary flower” plots (18 x 18 m) were established. Alyssum seedlings (Lobularia maritima var. ‘New Carpet of Snow’) were planted, with a spacing of 45 x 90 cm, 24 days after broccoli transplant. One of the blocks was set 90 m from one end of the strip, and the other 90 m from the other end, with a distance of 180 m between the two flower blocks.
Broccoli crop plants were sampled for arthropod abundance every 10 m from 0 to 80 m in the North and South directions from each flower plot. We visually examined six randomly-selected broccoli plants from evenly spaced rows in the 16 middle rows (rows 3, 6, 9, 12, 15, and 18) in each 10 m section of the 18 x 400-m no-aphicide block. Crop plants were sampled every 4-6 days from 19 days after broccoli transplant (= 5 days pre-alyssum transplant) until broccoli harvest. Each plant chosen in the 10 m section had its 6 largest leaves examined for the following pests and natural enemies: hoverfly eggs and larvae, cabbage aphid (CA), green peach aphid (GPA), potato aphid, imported cabbage worm (ICW), cabbage looper, diamond back moth, hoverfly larvae and eggs, cecidomyiid larvae and eggs, parasitized aphid mummies, spiders, lady beetles and lacewings. Herbivorous pests were further categorized into developmental stage.
The abundance of aphids, parasitized aphid mummies and hoverfly eggs at different distances from the flower plots were also sampled using bait plants of potted broccoli containing cabbage aphid colonies. These plants were produced in the greenhouse by forming aphid colonies of 10-30 apterous individuals within 13 mm diameter clip cages on 3 leaves on 3 week old broccoli seedlings in 4 l pots. These pots were then buried in the ground at distances of 0, 1, 5, 10, 20, 40 and 80 m from the flower plots along transects radiating in all 4 compass directions (there was only room for 40 m transects in each of the eastward transects however). Bait plants were left out in these transects for 3-5 days, then all aphids and hoverfly eggs were counted and recorded. All leaves containing aphids for each plant were then placed in a paper bags, allowed to sit for one week to permit the formation of mummies, and then placed in the freezer to prevent eclosion of parasitic wasps before the mummies were counted. Bait plants were placed out for a total of 8 rounds, starting 15 days after broccoli transplant and ending at harvest. All hoverfly eggs encountered on both crop and bait plants were collected, photographed and placed in Petri dishes with moist cotton wool and aphids to identify the hoverfly species depositing the eggs, once development was complete.
To measure the presence of adult flies, transects of yellow pan traps (18 cm diameter Solo® plastic bowls painted with Rustoleum® ‘safety yellow’) were placed in transects oriented identically to the bait plants. Pan trap height was kept within 15 cm of the upper broccoli canopy surface. Adult hoverflies and ladybird beetles were collected from each trap and stored in 70% alcohol, recording the number of trap-days. Pan traps were placed over a total of 9 rounds, from 15 days after broccoli transplant until harvest. Yellow sticky traps (2-sided, 18 x 40 cm) were staked in the same transects for one round, the week prior to harvest. Sticky trap height went from 20 cm below to 20 cm above the upper canopy surface. To check if the two types of yellow traps were collecting different species of hoverflies in equivalent proportions to those seen in the field, the alyssum flowers were observed on a weekly basis by both stationary and ‘census’ walking methods of observation.
Just before harvest, mature broccoli heads were randomly selected in the same grid described above for the crop plant sampling, for a total of 192 heads. Each head was examined for 5 minutes by destructive sampling of the heads into pieces smaller than 1cm3.
Analysis. The analysis of the crop and bait plant data will be by multiple linear regression, with hoverfly egg number as the response variable and distance from flowers and aphid number as the main explanatory variables. Explanatory variables of block, direction of sampling transect, and date, will also be considered for the analyses. The pan trap data will be analyzed by simple linear regression with distance, block, transect direction and date, as the explanatory variables. To see if the response varies by type of hoverfly species, a multivariate analysis of the different eggs types sampled will also be considered.
Sub-Objective 2. To evaluate the prey-finding and oviposition behaviors of adult hoverflies in commercial broccoli fields.
The same two field experimental sites at Stahlbush Island Farm described for Objective 1 above were used in this objective.
Research Questions and hypotheses. The oviposition behavior of hoverflies in relation to the aphid distribution on each sampled broccoli plant in the field was assessed according to the following observational research questions: 1) How many aphids per leaf, or per plant, are needed before hoverfly eggs are seen? 2) At what aphid densities are the peak numbers of hoverfly eggs observed? 3) If these thresholds and peaks exist, do they vary by hoverfly species, by aphid species, by aphid colony type, by field site, or over time? 4) Does this oviposition response vary on different parts of the broccoli plant?, and 5) How are the different aphid species distributed on different parts of the broccoli plant, especially at the end of the season?
Methods. Data were collected in two 15 x 66 m rectangles of broccoli, untreated with aphicides, at each of the two fields. Sampling began 25 days after broccoli transplant, and was repeated every 4 days until harvest. In each rectangle, every leaf on 50, randomly selected, broccoli plants was examined for the presence of all aphid species, hoverfly eggs, and the other key arthropods mentioned above in the methods for ‘Objective 1’. The numerical rank position of each leaf (starting from the center and radiating out to the lower leaves) was also recorded. At the 10-leaf stage of broccoli plant development, data from each leaf of each plant were recorded in separate categories of ‘inner’ (leaves closest to head under 6cm2), ‘middle’ (leaves next closest to head over 6 cm2), and ‘lower’ (leaves closest to ground which had begun to senesce).
Analysis. The analyses of these data will also be through multiple linear regression, with number of hoverfly eggs as the response variable and numbers of aphids per leaf and per plant as the main explanatory variables. Aphid species, aphid colony type, field site and leaf location on plant will also be considered as explanatory variables in additional analyses. Data analysis are incomplete at this stage.
Sub-objective 3. To evaluate the ability of local hoverfly species to limit populations of aphids in controlled conditions.
Hoverfly culturing. An adult hoverfly rearing facility was established in a greenhouse during spring and summer, 2002. Hoverflies were collected from various sites in the field. They were then placed in 1m3 mesh cages containing various combinations of: aphid species (cabbage aphid, green peach aphid and pea aphid), aphid plant hosts (broccoli, collards, brussels sprouts, kale, radish, bell beans, bush beans and peas), floral resources (alyssum, coriander, phacelia, buckwheat), artificial food resources (sugar cubes, honey, hazel pollen, oak pollen, grass pollen, bee-collected pollen, commercial protein extract and sugar water), as well as temperature.
Certain fly species survived cage conditions and oviposited on aphid-bearing plants. These plants were then placed in covered buckets where subsequent larval and puparial development was tracked, while adding additional aphid food as needed. Those flies that eclosed from puparia in the buckets were then placed in cages with other eclosed flies of the same species to see if mating and another round of oviposition would occur.
Ten species of hoverflies were collected, demonstrating differential abilities to survive, oviposit on aphid-bearing plants, develop into adults, mate, and repeat the cycle. Those species that have made it through a complete life cycle under artificial conditions to date are Eupeodes fumipennis and Sphaerophoria sulphuripes, two primary predacious hoverfly species found feeding on aphids in broccoli.
The relative aphid killing efficiency of 4 species of hoverfly was compared in a series of experiments. Three of these species Eupeodes fumipennis, Syrphus opinator, and Sphaerophoria sulphuripes, commonly attack cabbage aphids in large, commercial broccoli fields in this area. The fourth species Scaeva pyrastri, is one of the most species attacking cabbage aphids on garden plants in this area.
Methods
Multi-generation colonies of each of these species were established in the greenhouse to obtain the large numbers even-aged, naive larvae necessary for experimentation. Three initial experiments with aphids and hoverfly larvae on potted plants in 5-gallon bucket cages were performed, but reliable comparisons of killing efficiency among these species could not be obtained due to the habit of some species to crawl off of the plants (and away from the aphids) for prolonged periods. To achieve a more objective comparison among species, subsequent tests on killing efficiency and voracity were run in Petri dishes in the lab.
For these trials, a first instar hoverfly larvae from the same cohort was placed in a 10 cm diameter Petri dish with counted and weighed amounts of cabbage aphids. The dishes were covered, but not sealed to the outside environment, which was controlled for temperature and relative humidity. The number of living and dead cabbage aphids, the change in aphid weight, and the change in hoverfly larval weight were recorded each day. To obtain observations on the relative maximum voracity and killing efficiency of each species, aphids were added to each dish in excess of the amount needed each day. The maximum and minimum amounts of aphid needed per day per unit body weight of hoverfly larvae was assessed with preliminary experimentation. Aphid mortality in the dishes under these conditions without the presence of predators was found to be negligible.
Based on the availability of sufficient numbers of even-aged first instar larvae, 2 experiments were performed. The first experiment compared 6 replications of E. fumipennis, S. opinator and S. pyrastri over a period of 2 weeks. The second experiment compared 10 replications of E. fumipennis, S. opinator and S. sulphuripes over 4 weeks.
Objective 3. To develop a multi-faceted educational program for growers and agricultural professionals on integrating beneficial insectary plantings into various kinds of farming operations to enhance biological pest control.
An outreach program in conservation biological control (CBC) has developed as a partnership between the OSU Integrated Plant Protection Center and Oregon Tilth (Temporary Internet site: http://oregonipm.ippc.orst.edu/Agroecology/CBC_project.htm). This project falls within the “Biological Control and Biologically-Based pest Management” theme of the statewide IPM program that is coordinated within the IPPC (IPPC 2004, Jepson, 2003). The purpose of this activity is to develop a grower-based program in conservation biological control (CBC), facilitated by research and outreach at OSU.
This partnership will be based upon the principles of Community IPM. Community IPM, which was initially defined and elaborated by the FAO, incorporates IPM in a strategy for local, sustainable agricultural development, where farmers:
act on their own initiative and analysis; identify and resolve relevant problems; conduct their own local IPM programs that include research and educational activities; elicit support from local institutions; establish or adapt local organizations that include farmers as decision makers; employ problem-solving and decision-making processes that are open and egalitarian; create opportunities for all farmers in their communities to participate and benefit from the IPM activity; and promote a locally sustainable agricultural system.
Based upon these principles, the OSU CBC program is developing grower- to-grower information exchanges, carrying out farm walks and demonstrations of techniques, and establishing the basis for farm planning that can incorporate CBC practices through a process of on farm experimentation and evaluation.

Research results and discussion:

Objective 1. To evaluate the relative attractiveness of selected insectary plants to entomophagous arthropods and key insect pests
Each of the four insectary plants demonstrated varying degrees of attractiveness to key arthropod natural enemies and pests (Figs. 1 – 2).
The predatory hoverfly species observed at the North site included: Eupoedes fumipennis, Sphaerophoria sulphuripes, Syrphus opinator, Toxomerus spp., Platycheirus siegnus, P. quadraticus and Melanostoma mellinum. The non-predatory Syritta pipiens and Eristalis spp. were also abundant. Significantly more Sphaerophoria sulphuripes and total hoverflies were observed feeding on cilantro than the other 3 flowers (P < 0.05) at the North trial (Fig. 1A). This was also true for total predatory hoverflies, although the difference between cilantro and buckwheat was not significant. Lygus, ICW and Diabrotica demonstrated a strong preference for phacelia over the other flowers at this trial (P < 0.05) (Fig. 1B); the only exception being that the difference between phacelia and buckwheat for Diabrotica was not significant. More lady beetles were observed on buckwheat than alyssum and phacelia (P < 0.05), but not more than cilantro (data not shown).
The hoverfly community observed at the South site was similar to that described for the North site, only with fewer S. sulphuripes and more Syritta pipiens and Eristalis spp. At the South trial (Fig. 2A), a different pattern of hoverfly preference and feeding behavior was observed in that Eupoedes fumipennis displayed a significant preference for phacelia and alyssum over cilantro (P < 0.05). All of the observed feeding on cilantro was by the abundant members of the non-predatory genera Eristalis and Syritta. The preference of phacelia by the crop pest species observed in the North trial was also seen in this trial, although to a lesser extent. Lygus clearly preferred phacelia and buckwheat to alyssum or cilantro (P < 0.05). Cilantro and alyssum were also less attractive to Diabrotica and imported cabbage worm moths than phacelia (P < 0.05).

Objective 2. To evaluate the potential of using beneficial insectary plants to enhance biological control of specific insect pests in broccoli production systems, including: the cabbage aphid complex and the worm complex.
2000 Research
The results of the inspection of broccoli heads at harvest for both trials are shown in Fig. 3. Of greatest interest to the producers in these histograms would be the ‘with worm’ and ‘> 50 CA’ categories. The ‘near’ treatment of each trial had 1% of the heads sampled containing a worm, the near treatment of the North trial had 3% of the heads with > 50 Cabbage Aphids. The last broccoli plant sampling (within one day of the harvest head sampling), showed 40% of the plants sampled in this plot to have > 50 cabbage aphids (Fig. 5A), indicating a relatively low percentage of existing large cabbage aphid colonies actually making it to the head.
Hoverfly eggs appeared in the plots of each site 40-45 days after transplanting, and the appearance of hoverfly eggs and larvae at both the North and South trials was timed closely with the onset of plants containing more than 50 Cabbage Aphids (Figs 5 & 6). This response of hoverflies to plants with greater than 50 aphids can also be seen when these hoverfly data are plotted against the occurrence of Green Peach Aphid, or of all aphids in the same 3 density categories (graphs not shown).
This same relationship was demonstrated when each plant containing hoverflies was quantified for aphids, showing that eggs were only found on plants with more than 50 total aphids (data not shown). When each leaf containing hoverflies was quantified for aphids, a clear threshold effect was not observed, as a fair number of leafs without aphids had hoverflies. However, the average number of hoverflies per leaf was much greater for leaves with more than 50 aphids (data not shown).
2001 Research

Subobjective 1. To quantify the within-field effect that added flowering plants have on the attraction and oviposition activities of hoverflies, and on the abundance of other arthropod natural enemies and herbivores in broccoli.
Crop plants. Hoverfly eggs first appeared in low numbers two to three weeks before harvest, but the greatest oviposition occurred during the last few sampling dates, within a week of harvest (Figs. 7 and 8). Fig. 8 also shows a trend of greater oviposition at distances closer to the flowers on the final sampling date. Through the rearing of collected eggs, the majority of eggs on all sampling dates were found to be either Eupeodes fumipennis or Sphaerophoria sulphuripes (data not shown).
Bait plants. Hoverfly eggs appeared about the same time on the bait plants as on the leaves of the broccoli crop (Fig. 9). However, the trend of greater oviposition on leaves at sampling points closer to the flowers was not observed on the latest dates for this sampling method. This was true for both blocks, and all transect directions (graphs not shown).
Pan traps. Hoverfly adults appeared in the pan traps in the broccoli crop only after the alyssum flowers were planted (Fig. 10). Large numbers were found in the traps by the 6th sampling date, two weeks later. At this time in the broccoli crop season, capture rate peaked at distances 5 m from the flowers, and gradually decreased out to 80 m. Traps at distances of 0 m and 1 m from the flowers also trapped fewer flies on this date.
More than 90% of the flies captured in the traps on this date were Toxomerus marginatus (data not shown). The data from the final three pan trapping dates has not been processed yet. Yellow sticky card traps did not capture local hoverfly species (sticky trap data not shown). Several species of ladybird beetles were captured in large numbers, but no distance relationship to flowers was observed. Green lacewings were trapped at distances close to the flower plots, but in lesser numbers than those seen for the ladybird beetles.
Insect Contamination in Broccoli Heads. Out of 192 broccoli heads sampled in the no-aphicide strip, only 7% contained aphids. Of these, 14 heads, none had more than 10 aphids. When these data are broken down by distance class, no effect with distance to flowers was seen (Fig. 11).
Objective 2. To evaluate the prey-finding and oviposition behaviors of adult hoverflies.
Processing of data collected for this objective in the 2 field trials in 2000 is continuing and certain trends are already evident. The dataset is large, consisting of aphid and hoverfly egg counts on each individual leaf on each sampled plant. The analysis should be complete in the spring of 2002. The information in Fig. 12 is included here to show one trend that has been observed in many of the sampling dates looked at so far, that is, plants with less than 50 aphids did not have hoverfly eggs. No such threshold has yet been seen for individual leaves, many leaves with no aphids had hoverfly eggs. No peaks in oviposition response have been observed per leaf or per plant, rather, what has been seen is a sustained increase in number of eggs with an increasing numbers of aphids (Fig. 6). Remaining data manipulations and analyses to address this objective are outlined in the ‘Future Work’ section below.
Objective 3. To evaluate the ability of local hoverflies to limit populations of aphids s in controlled conditions.
Greenhouse studies were conducted in 2002 to evaluate relative voracity of key hoverfly species to consume aphids. Data clearly showed that Eupeodes fumipennis consumed the greatest number of aphids in the shortest time period, however Syrphus opinator and Sphaerophoria sulphuripes were also shown to have high levels of consumption of aphid prey. These data clearly support the importance of the predators in aphid biological control.
First Experiment:
Both the daily and cumulative cabbage aphid mortality was greatest for S. pyrastri, and lowest for S. opinator (Fig. 13). Both S. pyrastri and E. fumipennis killed an increasingly large number of aphids each day until they formed puparia after 8 or 9 days. Syrphus opinator individuals showed this trend at a slower rate up until 9 days, but then began to kill fewer aphids per day in the subsequent week, and did not form puparia by the time the experiment was terminated at 2 weeks.
Second Experiment:
Eupeodes fumipennis killed aphids at a much more rapid rate both S. opinator and S. sulphuripes (Fig. 14). On average, E. fumipennis killed an increasingly large number of aphids only up to day 8, at which point most individuals reduced their feeding rate as they were preparing for puparial formation. The peak rate of aphids killed per day was similar to that seen for this species in the first experiment, but the cumulative number of aphids killed was somewhat higher. Syrphus opinator and S. sulphuripes showed less of a trend of increased aphids killed per day in the first week. The killing rate of these two species remained moderate to low over the subsequent three weeks, and only three individuals of S. sulphuripes formed puparia successfully. Since individuals of these two species were allowed to feed until death, the cumulative number of aphids killed ended up being higher than that for E. fumipennis, and twice as high for S. opinator in the first experiment.
Discussion
The first objective of quantifying the effect that added flowering plants have on the activity of predatory hoverflies was addressed by measuring the amount of: oviposition on crop plants, oviposition on bait plants, aphids on crop plants, aphids in broccoli heads, and trapped adult hoverflies at different distances from the flowering plants over most of the crop’s development.
Oviposition did not occur to any significant extent until just before (less than one week) broccoli harvest. Much lower levels of oviposition were recorded on both crop and bait plant leaves for the two weeks prior to this period. After the 2000 trial, we hypothesized that providing floral resources earlier in the crop season, and in greater amounts might induce earlier, and greater amounts of oviposition. The 2001 trial used more than 6 times as many flowers and were provided approximately one month earlier in the broccoli field. Although the onset of hoverfly oviposition occurred at the same time as that seen in the 2000 trials (i.e. 3 weeks prior to harvest), the relative proportion of plants with hoverflies was higher at the end of the season. Also, unlike the 2000 trials, oviposition on crop plants was generally greater at sampling points closer to the flowers.
This same trend, of reduced oviposition at distances greater from the flowers, was not seen with the bait plant sampling method however. These differences may not be surprising when the differences in plant quality, size and number between these two sampling methods are considered. Additionally, since the oviposition activities of predatory hoverflies throughout a crop field are also influenced by the relative amounts of aphid hosts at each sampling point, the most appropriate analysis of oviposition response as a function of distance from floral resources will also take into account the number of aphids present at each sampling point. Once these aphid data are included in the analysis, the spatial patterns of oviposition response on both crop and bait plant sampling points at different distances from the flowers may be different from that reported here.
These aphid data, once processed, will also be used to assess the indirect effect that the floral blocks may have on aphid infestations at varying distances from the blocks on the last few sampling dates. Indirect effects on aphid infestation in the broccoli heads were not seen. The very low incidence of aphid-infested broccoli heads at all distances from the flower blocks sampled in the field (in terms of both relative percentage of infested heads and number of aphids in heads) probably indicates that the overall infestation of the heads in this no-aphicide strip was insufficient to detect any distance relationship which may have occurred. Levels of other key arthropod herbivore pests and natural enemies on both crop and bait plants were also too low in the sampling area to identify any spatial or temporal relationship with the added flower blocks.
Although eggs of E. fumipennis, S. sulphuripes and Platycheirus spp. did not appear until 3-4 weeks after the alyssum flowers were transplanted, adults of at least some individuals of these species were trapped within days of flower transplant. The reason for this lag could be either insufficient egg maturation in hoverflies present on these early sampling dates, insufficient numbers and arrangements of aphids to elicit oviposition responses, or a combination of both of these. This will be investigated further by dissecting the ovaries of the preserved specimens trapped on each date to assess egg development over time. These data will then be compared to the information derived from the analysis of oviposition response to varying levels of aphids on crop and bait plant leaves over time, to assess the relative importance of each.
We are continuing to develop appropriate experimental methodology to examine the ability of locally-occurring hoverfly species to limit aphid populations on broccoli. Our success with hoverfly culturing, suggests that this experimental approach can be developed further. The early results demonstrated that a combination of glasshouse conditions and host plant quality (particularly the removal of most leaves) affect hoverfly larval survival. Attempts will be made to enhance microclimate, and to improve the colonization and survival rate of larvae, by using clip cages for an initial period of acclimation.
This technique is could provide valuable, quantitative insights into the rate and patterns of hoverfly predation, interactions with other predators, and the ability of hoverflies to limit aphid population growth and the colonization of broccoli heads. Studies of this type are expected to provide more accurate information than simple voracity studies in Petri dishes, which can only provide minimum and maximum feeding rates.

Research conclusions:

Late season predation of cabbage aphids by predacious hoverfly larvae may have an important impact on the suppression of this pest and preventing excessive contamination of broccoli heads by these pests. We have documented high numbers of predacious hoverfly eggs in broccoli prior to harvest and we have developed methods to identify the key predacious hoverfly species. In our field experiments to date, however, we have been unable to demonstrate an enhancement of biological control of aphids by planting blocks of insectary flowers either on the margin of the field or in within the fields. We have made significant steps in understanding the key aspects of oviposition behavior of Eupeodes fumipennis, Sphaerophoria sulphuripes and Syrphus opinator, the major predacious hoverfly species occurring in broccoli in Oregon. There seems to be an “oviposition threshold” of approximately 50 aphids per plant that is required before the adult female hoverflies will begin to lay eggs on broccoli plants.

Participation Summary

Research Outcomes

No research outcomes

Education and Outreach

Participation Summary:

Education and outreach methods and analyses:

Objective 3. To develop a multi-faceted educational program for growers and agricultural professionals on integrating beneficial insectary plantings into various kinds of farming operations to enhance biological pest control.
To date, three farm walks have been undertaken in 2003 and 2004 (brief details provided at http://oregonipm.ippc.orst.edu/Agroecology/CBC_project.htm ). Farms that provide illustrations of particular CBC approaches have been selected, in collaboration with Oregon Tilth. These include sophisticated insectary planting regimes, hedgerow establishment and field boundary management in vegetable farms, and insectary planting, cover cropping and field boundary management in pome and stone fruits. Walks combine natural enemy sampling and identification, with grower-led reviews of practices, and farm planning exercises. Two workshops have also been completed, reinforcing information from farm walks, with discussion and exercises, including farm planning.
Participants from approximately 40 farms have taken part in the walks and workshops, and groups of growers with an interest in evaluating different practices are being formed at present.
Jepson,P.C. (2003) Supplement to Oregon IPM Newsletter: Enhancements to the state-wide IPM program [online]. Oregon State University: Integrated Plant Protection Center. April, 2003 - [cited August 8th, 2003]. Available from Internet: http://oregonipm.ippc.orst.edu/Supplement%20to%201%20-%20IPM%20Poster.pdf
IPPC 2004b Oregon IPM Program Highlights July 2002-December 2003. Available on line at http://oregonipm.ippc.orst.edu/Oregon%20IPM%20Program%20-%20Highlights%20FY%2020033.pdf
Invited presentations on this research were presented to the National meetings of the Entomological Society of America in Ohio (2003), Fort Lauderdale, FL (2002), to the Agronomy Society of America national meeting in Minneapolis, MN (2000) and to the Oregon Sustainability Conference in Portland, OR (See below)
Invited Presentations:
Ambrosino, M., P. Jepson, J. Luna, and S. Wratten. 2003. Hoverfly plant resource management for enhanced aphid pest management in broccoli. National Meeting, Entomological Society of America, Cincinnati, OH.
Luna, J. M. 2002. Applying theory to practice in conservation biological control: Lessons from a model system using broccoli, cabbage aphids, and predacious hoverflies. National Meeting, Entomological Society of America. Fort Lauderdale, FL.
_____2001. Sustainable agriculture as part of working landscapes. Oregon Sustainability Conference, Portland, OR.
_____2000. Habitat management strategies to enhance conservation biological control. National Meeting, Amer. Soc. of Agronomy., Minneapolis, MN.
We are currently working on an OSU Experiment Station Bulletin on the identification of predacious hoverflies in Oregon farm land. We are also currently preparing four manuscripts to be submitted to refereed scientific journals within the next year. These include:
Spatial and temporal distribution of predacious hoverflies (Diptera: Syrphidae) and aphids (Homoptera: Aphididae) in a flower-enhanced broccoli field. (For Environmental Entomology)
The relative frequencies of flower visits by predacious hoverflies, other natural enemies and herbivores in select insectary plants. (For Environmental Entomology.)
The within-plant distribution of different aphid pest species in commercial broccoli and hoverfly oviposition response. (For Ecological Entomology)
Quantifying cabbage aphid predation by hoverflies (Diptera: Syrphidae). (For Journal of Economic Entomology)

Education and Outreach Outcomes

Recommendations for education and outreach:

Areas needing additional study

Experimental designs are needed to evaluate landscape level impacts of conservation enhancement practices which involve actively dispersing insects like hoverflies. Traditional replicated experimental designs are of limited value because of the dispersal range of this insect. Clearly the timing of availability of insectary flowers, the distribution and the quantity of the insectary flowers all potentially affect the potential attractiveness and utility of the insectary plant to the beneficial species. Since the hoverflies were coming into the broccoli fields as soon as there were flowers, but these early flies had full guts of pollen and fully developed eggs, it seems that the flies were not limited in the landscape surrounding that field. Future research might focus on other hoverfly resources the immediate landscape surrounding study fields.
We have shown the importance of selection of insectary plants to the relative attractiveness to both pests and natural enemies. Clearly more work is needed to examine possible differences in floral architecture, as reported by Patt et al. 1997, which affect differential availability to specific pest and natural enemy species.

Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the view of the U.S. Department of Agriculture or SARE.